Data from: Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialisation from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. A total of 3644 genes were associated with behavioural specialisation which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characterized by an upregulation of three Vitellogenin (Vg) genes, one of which, Vg-like A, was the most differentially expressed gene that was recently shown experimentally to control the switch from brood- to worker-care. The expression of Conventional Vg was unlinked to behavioural specialisation, age or fertility, which contrasts to studies on bees and some ants. Diversity in Vg/Vg-like copy number and expression bias across ants supports subfunctionalisation of vitellogenin genes and indicates that some regulatory mechanisms of division of labour diverged in different ant lineages. Simulations revealed that our experimental dissociation of co-varying factors reduced transcriptomic noise, suggesting that confounding factors could potentially explain inconsistencies across transcriptomic studies of behavioural specialisation in ants. Thus, our study reveals that worker gene expression is mainly linked to the worker's function for the colony and provides novel insights into the evolution of sociality in ants.

社会性昆虫的生态成功依赖于劳动分工，这种分工不仅存在于蚁后与工蚁之间，更广泛存在于工蚁群体内部。工蚁的行为选择——是负责育幼还是外出觅食——会受到年龄、繁殖能力与营养状态的共同影响，其中育幼工蚁通常更为年轻、繁殖力更强且体型更为健壮。本研究以长刺细胸蚁（Temnothorax longispinosus）的工蚁为研究对象，通过实验手段将行为特化与年龄、繁殖能力这两个共变变量分离开来，并分析这些参数与全虫体基因表达的关联。最终共鉴定出3644个与行为特化相关的基因，其数量是与年龄相关基因的10倍，更是与繁殖能力相关基因的50倍。育幼工蚁的基因表达特征表现为三个卵黄蛋白原（Vitellogenin, Vg）基因的表达上调，其中Vg-like A的表达差异最为显著，此前已有实验证实该基因可调控工蚁从觅食状态向育幼状态的行为转换。常规卵黄蛋白原（Conventional Vg）的表达水平与行为特化、年龄或繁殖能力均无关联，这一结论与蜜蜂及部分蚂蚁的相关研究结果相悖。不同蚂蚁类群中Vg/Vg-like基因的拷贝数与表达偏好存在多样性，这一现象支持卵黄蛋白原基因发生了亚功能化，同时提示劳动分工的部分调控机制在不同蚂蚁演化谱系中产生了分化。模拟分析结果显示，本研究对共变变量的实验性分离有效降低了转录组数据的噪声，这表明混淆变量或许可以解释此前蚂蚁行为特化转录组学研究之间存在的不一致性。综上，本研究揭示工蚁的基因表达主要与其在蚁群中的职能密切相关，同时为蚂蚁社会性的演化提供了全新的认知视角。